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Contents lists available at SciVerse ScienceDirect
r.co
Developmen
Developmental Biology 369 (2012) 1931biosynthesis, auxin
metabolism, and auxin transport. Moreover,E-mail address:
[email protected] (C. Finet).From auxin biosynthesis to
signaling in the angiospermArabidopsis thaliana
Auxin pathway is controlled at many levels that include
auxin
0012-1606/$ - see front matter & 2012 Elsevier Inc. All
rights reserved.
http://dx.doi.org/10.1016/j.ydbio.2012.05.039
n Correspondence to: R.M. Bock LaboratoriesSean Carroll
Laboratory, Univer-
sity of Wisconsin, 1525 Linden Drive, Madison, WI 53706, USA.in
response to variable environmental cues. Phenotypic plasticityin
plant development might therefore constrain evolution in avery
different way from animals insofar as the nal shape of the
development, except when data about their role in developmentare
available (e.g., Arabidopsis or Physcomitrella).are thus able to
develop reiterative morphological units through-out the entire
lifespan. These modular units can also vary in form
plan in land plants. Due to the lack of functional data in
mostmodel species, this review mainly focuses on genes rather
thboth early in embryonic development and during all the life
cycle.Embryogenesis generates the apicalbasal axis, the radial
axis, thecotyledons (embryonic leaves) and the primary shoot and
rootmeristems. During postembryonic development, these
meristemsproduce lateral organs along the growing primary body axis
andestablish the proximaldistal axis. In contrast to animals,
plants
logous recombination.It is therefore timely to review our
understanding in the
evolutionary genetics of development across the land plants.
Herewe attempt to survey a limited number of recent ndings
thatinvestigate the extent to which changes in auxin signaling
couldhave played a role in the radiation and diversication of the
bodyIntroduction
Body plan (or Bauplan in Germafor the way the body of an
organisthe basic features for a phylum witone particular species of
that divisioan alternation of generations wheregametophyte (n) are
independent oized by a unique body plan. Themainly includes the
establishment oapicalbasal, the radial, and the pdetermination of
cell fate by positio
In seed plants, the principal bodysentially the blueprintid out.
It recapitulatesrecisely describing anyke animals, plants
haveorophyte (2n) and thems that are character-ing of the body
planproperties (such as theldistal axes) and theormation.of plants
are patterned
phytohormone auxin. Moreover, auxin mediates plant growth
inresponse to environmental signals. Thus, the evolution of
auxinhomeostasis and response systems is thought to play a key role
inthe evolution of land plant architecture (Cooke et al., 2004,
2002).
Coincident with the increased understanding of the
auxinsignaling in model organisms has been the development of
toolsand data in non-seed plants. The recently sequenced genomes
ofthe moss Physcomitrella patens (Rensing et al., 2008) and
thelycophyte Selaginella moellendorfi (Banks et al., 2011)
makecomparative genomic approaches possible. In parallel,
severaltools for studying gene function have been developed in P.
patens,such as RNAi, inducible promoters and gene targeting by
homo-In angiosperms, all these major patterning events involve
theReview
AUXOLOGY: When auxin meets plant e
Cedric Finet a,n, Yvon Jaillais b
a Howard Hughes Medical Institute and Laboratory of Molecular
Biology, University ofb Laboratoire de Reproduction et
Developpement des Plantes, INRA, CNRS, ENS de Lyon
a r t i c l e i n f o
Article history:
Received 6 March 2012
Received in revised form
9 May 2012
Accepted 31 May 2012Available online 9 June 2012
Keywords:
Hormone auxin
Signaling
Morphology
Plant
Evo-devo
a b s t r a c t
Auxin is implicated throu
hormone have been recogn
been shed on the molec
crosstalk with other horm
established a molecular fr
recent advances in auxin
morphology. By analogy
metazoan evolution, we pr
auxin in plant evo-devo.
journal homepage: www.elsevie-devo
consin, 1525 Linden Drive, Madison, WI 53706, USA
iversite de Lyon, 46 allee dItalie, 69364 Lyon Cedex 07,
France
ut plant growth and development. Although the effects of this
plant
d for more than a century, it is only in the past two decades
that light has
r mechanisms that regulate auxin homeostasis, signaling,
transport,
l pathways as well as its roles in plant development. These
discoveries
work to study the role of auxin in land plant evolution. Here,
we review
ogy and their implications in both micro- and macro-evolution of
plant
he term hoxology, which refers to the critical role of HOX genes
in
se to introduce the term auxology to take into account the
crucial role of
& 2012 Elsevier Inc. All rights
reserved.m/locate/developmentalbiology
tal Biology
-
auxin was proposed to act as an integrator of the activities
ofmultiple plant hormones, altogether suggesting a vast
regulatorynetwork of auxin during plant development (Jaillais and
Chory,2010).
Auxin biosynthesis
Indole-3-acetic acid (IAA) is the most potent naturally
occur-ring member of the auxin family. High IAA levels are detected
inshoot and root meristematic tissues, in cotyledons, as well as
inyoung leaves that have the highest biosynthetic capacity (Ljunget
al., 2001). In mature leaves and roots, IAA remains present butin
smaller amounts.
The identication of molecular components of IAA biosynthe-sis
revealed the existence of at least two separate major path-ways.
One is dependent on the precursor tryptophan (Trp) andthe other is
Trp-independent (see the review by Woodward andBartel, 2005).
Indeed, labeling experiments suggest that seedlingsdo not
synthesize IAA solely from Trp (Normanly et al., 1993).Moreover,
trp2-1 and trp3-1 mutants in Trp biosynthesis containcomparable
levels of free IAA to that of wild-type plants, suggest-ing that a
Trp-independent pathway occurs in plants. Analyses of
that the IAOx pathway is clade-specic and therefore might notbe
relevant at a macroevolutionary scale (Sugawara et al., 2009)(Table
S1).
Recently, two independent genetic screens revealed theimportance
of IPA in auxin biosynthesis (Fig. 1A). Both screensidentied
mutants in a tryptophan aminotransferase called TAA1that converts
IPA into indole-3-acetaldehyde (Stepanova et al.,2008; Tao et al.,
2008). Multiple mutants that disrupt three genesfrom the TAA1
family are severely impaired in both embryonicand post-embryonic
development and they have phenotypesreminiscent of auxin signaling
or transport mutants (Stepanovaet al., 2008). The IPA pathway was
recently shown to be veryshort, as IPA is directly converted into
IAA by avin mono-oxygenases from the YUCCA family (Fig. 1A)
(Mashiguchi et al.,2011). Plants overexpressing YUCCA genes contain
elevated levelsof free auxin and display auxin overproduction
phenotypes, aphenotype that is dependent on TAA1 activity
(Stepanova et al.,2011; Won et al., 2011; Zhao et al., 2001).
yuc1yuc4yuc10yuc11quadruple mutants lack a hypocotyl, a root
meristem and oralorgans, a phenotype very similar to some signaling
or transportmutants (Cheng et al., 2007a). YUCCAs are rate-limiting
enzymesin auxin biosynthesis and their expression is highly
regulated by
vDeg
Ret
aux
GA
P2A
sis,
C. Finet, Y. Jaillais / Developmental Biology 369 (2012)
193120the trp2-1 mutant imply that IAA could be produced from
indole-3-glycerol phosphate or indole (Ouyang et al., 2000).
In Arabidopsis, it is possible to distinguish two
Trp-dependentpathways: the indole-3-acetaldoxime (IAOx) pathway and
theindole-3-pyruvate (IPA) pathway. The IAOx pathway is carried
outby the two P450 monooxygenases CYP79B2 and CYP79B3.
Over-expression of CYP79B2 leads to an increase in free auxin
levelsand displays auxin overproduction phenotypes (longer
hypoco-tyls, epinastic cotyledons), whereas cyp79B-decient
mutantshave reduced levels of IAOx and IAA associated with
shorterpetioles and smaller leaves (Zhao et al., 2003). The
intermediateIAOx can be converted to IAA either by the enzyme
aldehydeoxidase protein AAO1 or indirectly by entering the
indolicglucosinolates pathway in which the last step consists in
hydro-lyzing indole-3-acetonitrile (IAN) to IAA. The P450
monooxygen-ase CYP83B1, the C-S lyase SUR1 and the IAN nitrilases
NIT1-3have been shown to be involved in the latter pathway (Bak et
al.,2001; Mikkelsen et al., 2004; Normanly et al., 1997).
However,CYP79B genes are not conserved outside of Brassicales and
IAOxintermediates are not found in rice, maize and tobacco,
suggesting
PID
GNOM
auxin
phosphoPIN
PIN
auxinCK
PTRP
IPA
IAA
TAA1
YUCCAIBAIAA-
conjugateGH3PIN5
ER
Nucleus
P
ABP1 PILS
Fig. 1. Schematic representation of auxin signaling: (A)
biosynthesis and homeosta
Auxin Response Element.both environmental and developmental
pathways. For example,the PIF transcription factors, which are
master regulators of light-mediated development, control elongation
by directly regulatingYUCCA genes transcription (Hornitschek et
al., 2012; Li et al.,2012; Sun et al., 2012). Besides, the
transcriptional activatorSTYLISH1 promotes leaf and ower
development by directlybinding to the YUCCA4 promoter (Eklund et
al., 2010a).
Auxin transport
In plants, two distinct pathways are known to play a role
inauxin transport: a passive distribution through vascular tissue
andan active cell-to-cell polar transport. This polar auxin
transport isfundamental for auxin distribution over both short and
longdistances. This transport occurs in a cell-to-cell manner
anddepends on specic inux and efux carrier proteins that
facilitatethe uptake and release of auxin from/to the apoplast
(Fig. 1B).Many auxin carriers are well characterized: the
PIN-FORMED (PIN)proteins (Galweiler et al., 1998) and several
proteins of the ABCBand ABCG transporter family (Cho et al., 2007;
Geisler et al., 2005;
Lyticacuoleradation
romer
inAUX1
Cell Wall
ABC
Nucleus
ABP1
ROP
AuxREARF+
Aux/IAA TPL
AuxREARF+
auxinIAA
AFB26Sproteasome
endocytosis
auxin
Low auxin
High auxin
ARF-
(B) polar auxin transport and (C) perception. GA, gibberellin;
CK, cytokinin; auxRE,
-
C. Finet, Y. Jaillais / Developmental Biology 369 (2012) 1931
21Ruzicka et al., 2010) are involved in auxin efux from the cell
andthe AUX1/LIKE AUXIN PERMEASE (AUX1/LAX) proteins areinvolved in
auxin inux (Bennett et al., 1996; Swarup et al., 2001).
Among these carriers, PIN proteins have been proposed tobe
central rate-limiting components in polar auxin transport(Petrasek
et al., 2006; Wisniewska et al., 2006). A key character-istic of
these proteins is their polar localization in the cell(Fig. 1B).
This polar localization correlates with putative auxinuxes in the
plants and are key to establish local auxin concen-trations
(Wisniewska et al., 2006). The processes behind theestablishment
and maintenance of PIN polarity at the cell levelare extremely
complex and rely on connections with the cell wall,the actin
cytoskeleton, phosphoinositide and calcium signaling,slow diffusion
in the plasma membrane as well as intracellulartrafcking (Fig. 1B)
(Dhonukshe et al., 2008a; Kleine-Vehn et al.,2011; Mravec et al.,
2011; Zhang et al., 2011). A determinantfactor for PIN polarity is
their endocytic trafcking. The currentmodel proposes that PIN
proteins are secreted in a non-polarmanner and that their
subsequent endocytosis and recylingestablish their polar
localization at the rootward pole of the cell(Dhonukshe et al.,
2008b). This polar recyling is dependent on theendosomal protein
GNOM (Geldner et al., 2003; Kleine-Vehnet al., 2009).
Phosphorylation of PINs by several kinases, includingPINOID (PID),
targets these auxin carriers to a GNOM-indepen-dent recycling
pathway that target them to the shootward poleof the cell (Fig. 1B)
(Kleine-Vehn et al., 2009). This action isantagonistically
controlled by the regulatory subunit of proteinphosphatase 2A
(PP2A) (Fig. 1B) (Michniewicz et al., 2007).
Endocytosis and recycling also control the quantity of
PINprotein at the plasma membrane by regulating the balance
ofprotein that is recycled back to the plasma membrane or
targetedto the lytic vacuole for degradation (Fig. 1B) (Abas et
al., 2006;Jaillais et al., 2006, 2007). The retromer, a conserved
proteincomplex, is involved in this balance as it promotes the
retrieval ofPIN proteins from late endosomes and reroute them
toward theplasma membrane (Fig. 1B) (Jaillais et al., 2007). Auxin
itself playsa key role in this regulation as it can inhibit
endocytosis at certainconcentration or promotes PIN proteins
degradation at others(Abas et al., 2006; Paciorek et al., 2005;
Robert et al., 2010).Moreover, MAB4/ENP/NPY1 and its closest
paralogs were recentlyshown to control polar auxin transport and
PIN protein localiza-tion as well as their quantity at the plasma
membrane (Chenget al., 2007b; Furutani et al., 2007, 2011; Li et
al., 2011). Similarlyto the PINs, MAB4/ENP/NPY1 family proteins are
polarly localized.However it is still unknown how they regulate PIN
intracellulartrafcking. They belong to a plant specic family of 33
membersthat includes NPH3, a protein partner of the phot1 blue
lightphotoreceptor involved in phototropism (Christie, 2007;
Pedmaleand Liscum, 2007). NPH3 was recently shown to function as
asubstrate-specic adapter in a CULLIN3-based E3 ubiquitin
ligase(Roberts et al., 2011). As such, NPH3 can promote mono-
andpoly-ubiquitination of phot1, which modify both its
subcellularlocalization and quantity at the plasma membrane
(Robertset al., 2011). It has been recently shown that
monou-biquitinationcontrols membrane protein trafcking in
Arabidopsis (Barberonet al., 2011) and that PIN2 is ubiquitinated
in planta (Abas et al.,2006; Leitner et al., 2012). Taken together,
it is tempting tospeculate that MAB4/ENP/NPY1 might modulate PIN
proteinlocalization by a ubiquitination-dependent regulation of
theirintracellular trafcking.
Other mechanisms controlling auxin levels and homeostasis
As discussed above, maintenance of correct cellular auxinlevels
requires biosynthesis and transport. Another important
regulation level is auxin storage as inactive conjugates
andindole-3-butyric acid (IBA), which can provide free IAA
uponhydrolysis and b-oxidation, respectively (Fig. 1A). Hence, IAA
canbe ester-linked to sugars or amide-linked to amino acids
leadingto a great diversity in IAA conjugates (reviewed in
Woodwardand Bartel, 2005). Remarkably, the conjugation to amino
acidsinvolves enzymes of the GH3 family, whose members have
beenidentied as early auxin responsive genes (Abel and
Theologis,1996), suggesting that auxin levels are maintained in
part by anegative feedback loop (Fig. 1A). Overexpression of GH3.2
(YDK)or GH3.6 (DFL1) results in phenotypes consistent with
decreasedfree auxin levels, such as reduced lateral roots and
hypocotylelongation (Nakazawa et al., 2001; Takase et al., 2004).
Contraryto GH3 enzymes, IRL1/ILL amidohydrolases carry out the
releaseof free IAA from conjugates (reviewed in Ludwig-Muller,
2011).Noticeably, there is evidence that some of the auxin
conjugatessuch as IAA-aspartate and IAA-glutamate are intermediates
inIAA degradation rather than storage conjugates (reviewed
inLudwig-Muller, 2011).
It was recently shown that PIN5, contrary to other PINs, is
notlocalized at the plasma membrane but is localized at the
surfaceof the endoplasmic reticulum (ER) (Fig. 1A) (Mravec et al.,
2009).PIN5 might mediate auxin ow from the cytosol into the lumen
ofthe reticulum and therefore might modulate intracellular
auxinhomeostasis by limiting the auxin availability for
cell-to-celltransport or nuclear signaling. PIN8 is also an
atypical PIN thatis localized in the ER and controls auxin
homeostasis in pollen(Bosco et al., 2012; Ganguly et al., 2010;
Mravec et al., 2009).Besides, a family of PIN-LIKES proteins (PILS)
also localized inthe ER was recently described as regulators of
intracellular auxinhomeostasis (Barbez et al., 2012). Taken
together, these resultsshow that the conjugation/hydrolysis and
storage of IAA istherefore a central way to regulate auxin
concentration at thecellular level.
Auxin perception and signaling
The transcriptional auxin signaling pathway is mainly mediatedby
the auxin co-receptors of the TIR1-AFB family (Dharmasiri et
al.,2005; Kepinski and Leyser, 2005), the auxin signaling
repressorsof the Aux/IAA family, the transcription factors of the
AUXINRESPONSE FACTOR (ARF) family, and the transcription
co-repressorTOPLESS (TPL) (Fig. 1C) (Szemenyei et al., 2008). In
absence of auxin,Aux/IAA form a trimeric complex, presumably onto
DNA, with DNA-binding ARF proteins and the transcriptional
co-repressor TPL(Szemenyei et al., 2008), thus repressing the
transcription ofauxin-induced genes (Fig. 1C, top) (Ulmasov et al.,
1997). Auxininteracts both with TIR1/AFBs and Aux/IAA proteins
acting asmolecular glue between the two proteins (Dharmasiri et
al., 2005;Kepinski and Leyser, 2005; Tan et al., 2007). Auxin
thereforepromotes Aux/IAAs ubiquitination by TIR1/AFBs E3-ubiquitin
ligasesand subsequent degradation by the proteasome (Dharmasiri et
al.,2005; Kepinski and Leyser, 2005). Different combinations of
TIR1/AFB and Aux/IAA proteins form co-receptor complexes with a
widerange of auxin-binding afnities that are mainly determined
byAux/IAA proteins (Calderon Villalobos et al., 2012). In the
absenceof Aux/IAA and TPL, ARFs can act as transcriptional
regulators(Fig. 1C, bottom) (Gray et al., 2001). ARFs can be
transcriptionalactivator (ARF) or repressors (ARF). It was recently
shown thatthe majority of activators ARFs interacts with most
Aux/IAAs, whilemost repressor ARFs do not or in a limited way
(Vernoux et al.,2011). This work suggests that repressor ARF
activity might beregulated independently of auxin and that they act
by competingwith activator ARFs for binding to TGTCTC auxin
responsive ele-ments (AuxREs) at promoters of auxin responsive
genes (Fig. 1C).Therefore, the respective concentration of ARF and
ARF might
inuence the threshold of auxin sensitivity in a given cell or
tissue.
-
those cells (Brunoud et al., 2012; Vernoux et al., 2011), as
well as
C. Finet, Y. Jaillais / Developmental Biology 369 (2012)
193122the auxin sensitivity based on the expressed
TIR/AFB-Aux/IAAco-receptor system (Calderon Villalobos et al.,
2012).
Another auxin receptor is the AUXIN-BINDING PROTEIN1(ABP1) that
binds auxin with high afnity and specicity (Hertelet al., 1972).
Plants overexpressing ABP1 exhibit an auxin-depen-dent expansion in
the size of differentiated cells that are normallyunresponsive
(Jones et al., 1998), whereas loss of ABP1 functioncauses embryonic
arrest and results in defects in cell division andcell elongation
(Chen et al., 2001). Moreover, inducible inactiva-tion of ABP1
affects plant growth by interfering with the cell cycleduring
postembryonic shoot (Braun et al., 2008; David et al.,2007) and
root (Tromas et al., 2009) development. ABP1 issecreted in the
lumen of the reticulum and found in the apoplast(Fig. 1A and C). It
is not clear how auxin binding to ABP1 istransduced, but it was
recently shown that ABP1 signaling couldact independently of the
TIR1/AFB system at a post-transcrip-tional level (Robert et al.,
2010; Xu et al., 2010). Indeed, auxinbinding to ABP1 inhibits
endocytosis, which among other effects(Fig. 1C), regulates the
amount of PINs at the surface of the celland therefore promotes its
own efux (Paciorek et al., 2005;Robert et al., 2010). Moreover,
ABP1 acts upstream of the smallGTPase of the RHO-OF-PLANT (ROP)
class in regulating cellmorphogenesis (Xu et al., 2010). However,
loss of ABP1 functionalso impairs the up-regulation of early auxin
responsive genes(Effendi et al., 2011; Tromas et al., 2009). So
far, it is unknownhow ABP1 is regulating gene expression and
further experimentsare required to determine whether there is a
signaling pathwayfrom ABP1 to the nucleus, perhaps implying ROP
GTPases (Xuet al., 2010) or whether this effect on auxin inducible
genes is theresult of feedback between ABP1 and TIR1/AFBs signaling
(Effendiet al., 2011).
A third pathway acting independently from TIR1 is mediatedby the
putative dual-specicity protein phosphatase INDOLE-3-BUTYRIC ACID
RESPONSE5 (IBR5). Mutations in IBR5 conferresistance to auxin and
result in decreased plant height, defectivevascular development,
and fewer lateral roots (Monroe-Augustuset al., 2003). Contrary to
the TIR1 signaling, Aux/IAA repressorproteins are not destabilized
after response to auxin through thispathway (Strader et al., 2008).
The targets involved downstreamof IBR5 are not yet identied.
Auxin: a key role in the development of owering plants
The polar auxin transport generates local auxin
concentrationsthat are instrumental in morphogenesis. Formation of
an auxingradient has been proposed to be necessary for cell
specicationwithin the root meristem (Blilou et al., 2005; Friml et
al., 2002;Grieneisen et al., 2007; Sabatini et al., 1999) and the
secondary xylem(Uggla et al., 1996), and to regulate planar
polarity in the root (Ikedaet al., 2009) as well as patterning of
the embryo sac (Pagnussat et al.,2009). Initially, these studies
suggest that auxin acts as a morphogen,conferring patterning
information in a concentration-dependentThe widely used synthetic
auxin-responsive promoter DR5 mighttherefore be seen as a reporter
of the ratio between acting ARF andARF in a cell rather than a
reporter for auxin as it is often referredto. A newly described
auxin sensor (DII-VENUS) consists of a fusionbetween the Aux/IAA
auxin interaction domain and the fast matura-ting uorescent protein
mVENUS (Brunoud et al., 2012). DII-VENUSis degraded when auxin is
perceived and is therefore a responseinput sensor, while the DR5
promoter monitors the output response.Direct comparison between
DII-VENUS and DR5 activity exempliesthat auxin perception is not
necessarily translated into gene induc-tion, which might in part be
due to the repressive activity of ARF inmanner. However in many
cases, the emerging view is that auxinacts more like a
threshold-specic trigger (Lau et al., 2011). Accordingto the
morphogen hypothesis, a given cell converts auxin gradientsinto
different cellular outputs given its position within the
establishedgradient. However in the threshold-specic trigger
hypothesis, auxindoes not necessarily have to establish a gradient
but to go above orunder a certain threshold concentration to induce
the morphogeneticevent. Therefore, the trigger concept is a
morphogen concept with adiscrete or one-step response. Thus, it is
often the establishment ofauxin maximum (Benkova et al., 2009) or
minimum (Sorefan et al.,2009) that is important for organogenesis.
Importantly, the auxinthreshold can be set at different levels
(Vernoux et al., 2011) andtrigger various cellular and
developmental outputs depending on thelocal signaling capacity of a
given cell (Brunoud et al., 2012), such asthe presence of different
Aux/IAA-ARF pairs (Rademacher et al., 2012),of different
Aux/IAA-TIR1/AFB co-receptors (Calderon Villalobos et al.,2012) or
the signaling state of other hormones (Nemhauser et al.,2004).
Polar auxin transport: from the cell to the tissue level
The establishment of auxin minima and maxima involves
thecoordination of auxin uxes at the tissue level. Several
experimentsand computer-based models have been proposed to explain
thelink between PIN protein distribution, local auxin
accumulationand cellular output. The canalization model proposes
that auxintransporters act by amplifying and stabilizing existing
auxin uxes,i.e., a positive feedback between ux and transport
(Sachs, 1969).The canalization model is both supported by
experimental data forthe formation of venation pattern (Sauer et
al., 2006; Scarpellaet al., 2006) as well as by simulation data for
the auxin uxes in theapical meristem (Stoma et al., 2008). More
recently, the extra-cellular receptor-based polarization (ERP)
model (Wabnik et al.,2010) proposes a mechanistic view of the
canalization model bytaking into account auxin feedback on PIN
transcription (Peer et al.,2004) and auxin feedback on PIN
endocytosis (Paciorek et al., 2005)through extracellular auxin
perception.
Alternatively to the canalization (or ux-based) model, the
up-the-gradient (or concentration-based) model proposes that cells
areable to sense auxin concentrations in surrounding cells and
subse-quently drive auxin against the gradient by directing plasma
mem-brane PIN proteins to the membrane adjacent to the neighboring
cellwith highest auxin concentration (Jonsson et al., 2006; Smith
et al.,2006). One remaining question is to understand how cells
could senseauxin concentrations in their surrounding environment. A
recentstudy reveals that biomechanics mediates the coupling between
PIN1localization and cortical microtubule orientation (Heisler et
al., 2010).By inducing cell growth and subsequent arrangement of
microtu-bules, auxin triggers the accumulation of PIN proteins at
the plasmamembrane adjacent to the expanding neighbor. Thus, the
sensor-cellexports auxin toward the expanding neighbor, both
increasing itsauxin concentration and mediating the feedback loop
between auxinand its transport.
Auxin and embryogenesis
Apicalbasal axis formation is tightly linked to dynamicchanges
in auxin concentration and ux (Fig. 2A) (reviewed inBowman and
Floyd, 2008). First, an asymmetric distribution of theefux carrier
PIN7 mediates auxin ow into the apical cell untilrst zygotic
divisions (Friml et al., 2003). Second, auxin is drainedfrom the
embryo due to asymmetric distribution of PIN1 duringthe globular
stage (Friml et al., 2003). Third, auxin ow is directedtowards the
top of the embryo through the protodermal layer, andthen downwards
through the center (Benkova et al., 2003; Frimlet al., 2003). Last,
reversal in PIN1 polarity at the apex of the
globular embryo denes a zone depleted in auxin: the future
shoot
-
intion
ma
uced
le, P
en.
C. Finet, Y. Jaillais / Developmental Biology 369 (2012) 1931
23apical meristem. Although the asymmetric distribution of
IAAcannot occur without polar transport, the relative importance
oflocal auxin production during embryogenesis has been revealedonly
recently. Multiple yuc mutants have severe embryo andcotyledons
defects (Cheng et al., 2007a; Stepanova et al., 2008,2011) and the
protein LEAFY COTYLEDON2, a key transcriptionfactor in embryo
development, has been shown to induce auxinresponses by binding
directly to the YUC4 promoter (Stone et al.,2008). In conclusion,
both convergent auxin ow and localizedauxin synthesis lead to the
creation of auxin maxima that cor-respond to future root meristem,
cotyledons and vasculature.
Local auxin accumulation activates the two transcription
factorsMONOPTEROS (MP)/ARF5 and NONPHOTOTROPIC
HYPOCOTYL4(NPH4)/ARF7 by degrading the Aux/IAA transcriptional
repressorBODENLOS (Hamann et al., 2002). MP and NPH4
maintainPLETHORA (PLT) gene expression in the basal region of the
develo-ping globular embryo. PLT transcription factors are
essential for
Putativeauxin fluxes
High auxconcentraor "auxin
Acropetal(rootward)
Basipetal(shootward)
Fig. 2. Pleiotropic role for auxin in plant development.
Putative auxin uxes as ded(A), root system (B) and lateral root
(C). PIN1 protein is in red, PIN3 protein is in purp
represented by red, purple and blue arrows respectively. Auxin
maxima are in grequiescent center specication and denition of the
stem cell nichein the root meristem (Aida et al., 2004). On the one
hand, theexpansion of PLTs gene expression into the progenitor cell
of thequiescent center is induced by auxin and relies on ARF action
(Aidaet al., 2004). In turn PLT genes trigger the expression of PIN
genesthat establish the auxin maximum in the root meristem,
therebyrestricting the expression of the PLT genes (Blilou et al.,
2005). Onthe other hand, PLT proteins are expressed in a gradient
pattern,which overlaps the auxin gradient, with highest expression
in thestem cell area, intermediate levels in the division zone, and
lowlevels in the elongation zone (Galinha et al., 2007). Taken
together,these results suggest that developmental gradients are the
result offeedback interactions in auxin signaling (Benjamins and
Scheres,2008).
Local auxin concentrations play also a role in establishing
theexpression patterns of key transcription factors in the
apicalregion of the embryo. For instance, the transcription factors
CUCare essential in creating boundaries into the developing
embryoof A. thaliana and their expression is correlated with low
auxinlevels (Furutani et al., 2004). The same correlation is
observed forclass I KNOX genes (such as SHOOT MERISTEMLESS) that
promotethe formation of the future shoot apical meristem in a
region oflow auxin concentration and low PIN-mediated transport
(Hayet al., 2006). In contrast, class III homeodomain-leucine
zippergenes have expression patterns that correlate with
knownpathways of auxin ow out of the apex toward incipient
leafprimordial and in the provasculature (Heisler et al.,
2005).
In conclusion, interplay between sites of auxin maxima andspecic
patterns of both auxin-responsive genes and other pat-terning genes
subdivide the embryo along both the apicalbasaland radial axes.
Auxin and postembryonic development
Shoot and root growth and development are a reiteration ofbasic
patterning processes established during embryogenesis(Benkova et
al., 2003). Thus, auxin continues to play a key rolein generating
postembryonic lateral organs.
The primary root usually branches to form lateral roots
thatextend horizontally from the latter one (Fig. 2B and C).
Lateralroots play a role in facilitating anchoring and absorptive
proper-ties of the plant. Lateral roots originate exclusively from
pericycle
PIN1 lateralization
PIN1 PIN7PIN3
xima"
from functional studies and localization of PIN proteins in the
developing embryo
IN7 protein in blue and the putative auxin uxes associated with
these carriers arefounder cells (Dolan et al., 1993) and their
initiation beginswhen either individual or pairs of pericycle
founder cells undergoseveral rounds of anticlinal divisions (Malamy
and Benfey, 1997).Every pericycle cell has the ability to divide in
response toelevated auxin levels (Boerjan et al., 1995). However,
only fewof these cells become founder cells. Auxin has been shown
toregulate spacing of pericycle founder cells by generating
auxinaccumulation sites in the protoxylem that prime the
adjacentpericycle cells to become founder cells (De Smet et al.,
2007).Local auxin accumulation causes the degradation of
IAA14,thereby releasing the repression on ARF7 and ARF19, and
allow-ing them to directly activate the expression of LBD/ASL18
andLBD/ASL16 transcription factors (Okushima et al., 2007).
Auxinplays therefore a crucial role in regulating lateral root
patterning(recently reviewed in Peret et al., 2009). Auxin also
acts as a localinductive signal that reprograms cells overlaying
lateral rootprimordia to facilitate organ emergence (Swarup et al.,
2008).Last, auxin could be necessary for the activation of the
lateralroot meristem and the elongation of the new primordium
(Peretet al., 2009).
As a last example, we would mention the key role of auxin inthe
patterning of the angiosperm female gametophyte. It has
beenrecently shown that auxin is implicated in polarizing the
femalegametophyte by creating a gradient-based distribution
(Pagnussatet al., 2009). Thus, auxin concentration determines cell
fates, with
-
the highest auxin levels specifying synergids, followed by egg
cells,and the lowest auxin resulting in antipodal cells.
Remarkably,this gradient does not seem to be established by polar
auxintransport but mainly by spatially differential activities of
YUCCAgenes (Pagnussat et al., 2009).
Auxin and crosstalk with other hormone pathways
Auxin interacts at many levels with all the other planthormone
pathways and therefore broadly impacts morphogenesis(Jaillais and
Chory, 2010). Most hormone pathways heavily affectauxin homeostasis
mainly by modifying expression of auxintransport, biosynthesis or
signaling components (Vert and Chory,2011). For example, cytokinins
induce the expression of IAA3, anegative regulator of the
auxin-signaling pathway at the transi-tion zone of the root,
thereby providing a frontier for auxin-induced cell proliferation
versus differentiation (Dello Ioio et al.,2008; Moubayidin et al.,
2010). Ethylene, too, controls auxinlevels by manipulating the
expression of both auxin transporters(from the AUX and PIN
families) and biosynthetic enzymes(for example, the auxin
biosynthesis enzyme TAA1) (Ruzickaet al., 2007; Stepanova et al.,
2008, 2007; Swarup et al., 2007).Additionally, auxin feeds back on
ethylene biosynthesis in acomplicated mechanism that controls the
auxin-ethylene levelin root cells.
A new emerging paradigm is the regulation of PIN
proteinstrafcking by other plant hormones. Indeed, cytokinins
wererecently shown to control PIN protein endocytosis and to
inducetheir degradation in lytic vacuoles (Fig. 1B) (Marhavy et
al., 2011).High concentrations of jasmonate also induce PIN2
endocytosisand degradation (Sun et al., 2011). On the contrary,
gibberellin
signaling and the secretory peptides from the GOLVEN familylimit
PIN trafcking to lytic vacuoles (Fig. 1B) (Whitford et al.,2012;
Willige et al., 2011). Therefore, not only auxin itselfregulates
its own efux, but also many other hormones controlthe intracellular
trafcking of PIN and therefore local auxinaccumulation required to
trigger morphogenetic events. Interest-ingly, some of these
regulations do not require transcription(Marhavy et al., 2011;
Robert et al., 2010). Therefore, there areat least two complex
regulatory networks involved in hormonecrosstalk in the case of
auxin, one transcriptional and one onthe regulation of PINs
intracellular trafcking, particularly on thebalance between
recycling and degradation.
Given that auxin is involved in numerous aspects of plantgrowth
and development, it is not surprising that auxin regula-tion turns
out to be so complex and so intertwined with that ofother plant
hormones. How these different levels of regulationelaborated during
the course of land plant evolution is conse-quently a fascinating
question and will be discussed in thefollowing section.
Evolution of the auxin pathway in land plants
Land plants (embryophytes) are thought to have evolved
fromancestral charophycean green algae (Finet et al., 2010b;
Graham,1993). Subsequently to the colonization of land,
embryophytesunderwent radiation and rapid diversication of body
plans. Themain features of body plans and phylogenetic
relationshipsamong extant phyla of land plants are illustrated in
Fig. 3. Auxinwas detected in virtually all branches of the green
lineage and ithas been clear for decades that all land plants
respond in dramaticways to auxin application (Cooke et al., 2002).
Moreover, auxin
liverwortsPhMa
Ph
Os
Se
ZeOr
ArAr
Ch
Ph
Gi
PiPi
NiCh1
s
quis
f the
con
C. Finet, Y. Jaillais / Developmental Biology 369 (2012)
193124charophytes
chlorophytes
Fig. 3. Evolutionary changes in auxin biology in green plants.
Key to characters: 1, acacquisition of the PIN proteins involved in
auxin efux and homeostasis; 4, acquisition o
IAA amidohydrolases; 6, predominance of
IAA-aspartate/glucose/glutamate over amideeudicotsmonocots
magnoliids
ANA grade
Gnetales
cycads
Ginkgo
monilophytes
lycophytes
hornworts
mosses
Coniferales I
Coniferales II
seed
root, leaf, vasculature
apical growth,
carpel
embryo
2 3
6
5
4conjugates hydrolysis. On the left, the presence () or absence
() of a given character is onaeoceros S -rchantia G +
yscomitrella
munda S +
laginella S +
lorella G -
+
yscomitrella GS
-+
++ +
nkgo S +
nuscea S +
S +
tellaara G
G -
-+
+
+
gymnosperm
sbryophytes
ition of the BTB-NPH3-like gene family; 2, acquisition of the
TPL/TPR gene family; 3,
ability for cells to store IAA by conjugation; 5, acquisition of
the ER-localized IRL1-like
jugates, some key enzymes involved in the release of free IAA
after IAA-amino acidayza
abidopsis SG
+abidopsis +
+ +- +
+ +
S + + +S + + +
angiospermly mentioned when it has been experimentally tested,
S: sporophyte, G: gametophyte.
-
C. Finet, Y. Jaillais / Developmental Biology 369 (2012) 1931
25ability to act as a morphogen could date back to the origin of
seedplants, as suggests the establishment of an auxin
concentrationgradient for the specication of secondary xylem during
woodformation in Scots pine (Uggla et al., 1996). However,
themolecular mechanisms underlying the biology of auxin in
early-diverged lineages of land plants remain elusive, as well as
wherein the ancestral charophycean lineage the components of
auxinbiosynthesis/transport/response were assembled.
Origin of auxin metabolism
With regard to the Trp-dependent pathway, the YUCCA genefamily
is ancient in land plants, with homologs identied inthe moss
Physcomitrella (Rensing et al., 2008) and the lycophyteSelaginella
(Banks et al., 2011). In order to tackle the overallpathway, we
conducted bioinformatic analyses of the availablegenomic data in
the plant kingdom. Most of the genes involved inIPA-dependent
pathway in owering plants are found in landplants (Table S1).
Although data are very sparse in marchantio-phytes and
anthocerotophytes, it seems likely that the Trp-dependent pathway
is very much the same in all land plants.Nevertheless, the
molecular function of these different genesremains to be
established in non-model species. Only the func-tional
characterization of PpSHI1 and PpSHI2 has been reported inP.
patens. The two PpSHI genes cooperatively induce IAA bio-synthesis
in the gametophyte (Eklund et al., 2010b). Althoughthere are hardly
any of these orthologs in algae, genes encodingthe putative
amidohydrolase AMI1, Trp-synthase a TSA1, and Trp-synthase b TSB1
have been identied in chlorophytes (Table S1).Since these enzymes
are involved in the indole-3-acetamide(IAM) pathway, auxin might be
synthesized via the IAM pathwayin algae as it occurs in
microorganisms (Patten and Glick, 1996).Finally, the
Trp-independent pathway is poorly characterized inmodel plants,
which limits evolutionary genomic approaches.
IAA conjugation seems to be a widespread process to controlfree
IAA levels in land plants (see the review by Ludwig-Muller,2011).
However, noteworthy differences stand about the nature ofmajor
conjugates that consists either in amide conjugates (liver-worts,
mosses, hornworts) or IAA-aspartate/glucose/glutamate(lycophytes,
ferns, seed plants). But the main striking feature isthe slow
conjugation rate in liverworts, suggesting that thestrategy
biosynthesis/degradation is predominantly used in thisphylum
(Sztein et al., 1999). Given that the biosynthesis/degrada-tion of
IAA is assumed to occur in charophyte algae, liverwortscould have
retained the putative ancestral strategy for controllingfree IAA
levels (Cooke et al., 2002). On the contrary, the otherphyla in
land plants evolved the potential to regulate free IAAlevels by
adjusting the equilibrium conjugation/hydrolysis. Theresults we
obtained using in silico methods corroborate onlypartially the
latter evolutionary schema. Indeed, group II GH3proteins are absent
from chlorophytes but present in all embry-ophyte lineages,
including marchantiophytes (Table S1). Hence, itwould be
interesting to test whether class II GH3 enzymes arecapable to
catalyze conjugation in species belonging to marchan-tiophytes.
Remarkably, like in owering plants, GH3 proteins actas auxin
conjugate synthetases in P. patens (Ludwig-Muller et al.,2009a,
2009b). Concerning hydrolysis, IRL1/ILL IAA amidohydro-lases are
present both in extant algae and land plants whereasconjugates
hydrolysis does not seem to occur in algae (Szteinet al., 1995).
IRL1/ILL IAA amidohydrolases could have beenrecruited later in the
land plants for controlling IAA free levels.
Origin of the polar auxin transport
Polar transport of auxin can be directly measured by tracing
radioactive synthetic IAA. Basipetal auxin transport was
thusreported in the sporophytes of mosses (Fujita et al., 2008;
Poliet al., 2003) and those of lycophytes (Wochok and Sussex,
1973).Besides, basipetal auxin transport was suggested to occur in
mossrhizoids (Eklund et al., 2010b; Rose and Bopp, 1983). On
thecontrary, no polar auxin transport was detected in moss shootsin
the gametophyte (Fujita et al., 2008). Both the inux and
efuxcarriers are sensitive to several inhibitors. The compounds
1-N-naphthylphthalamic acid (NPA) and 2,3,5-triiodobenzoic
acid(TIBA) have traditionally been used to inhibit the efux
componentof the polar auxin transport mechanism. Treatments with
auxintransport inhibitors cause changes in the putative
distribution ofauxin in the sporophyte and result in abnormal
embryo develop-ment (Fujita et al., 2008). On the contrary, no
changes are noticedin the haploid shoot (Fujita et al., 2008). To
conclude, the establish-ment of the apicalbasal axis in moss
sporophytes requires properdistribution of auxin during
embryogenesis. This patterning isensured by a mechanism of polar
auxin transport, the molecularcomponents of which are still poorly
known in P. patens. Genomicapproaches pinpoint the presence of
three and ve PIN homologsin the Physcomitrella (Rensing et al.,
2008) and Selaginella (Bankset al., 2011; Floyd and Bowman, 2007)
genomes, respectively.Although Physcomitrella PIN proteins share
characteristics withPM-localized PINs (a central hydrophilic loop
and a conserveddomain around the putative tyrosine motive NPNTY),
one of themis predominantly localized at the ER (Mravec et al.,
2009). The ERlocalization of one moss PIN protein suggests that the
function ofPINs in mediating auxin homeostasis was present in the
lastcommon ancestor of land plants. Some authors recently
proposedthat ER-localized moss PIN proteins could also play a role
ingenerating an intercellular auxin transport by ER-localized
auxintransporters (Wabnik et al., 2011). This putative ancestral
mechan-ism presumes that ER acts as an auxin reservoir and the
release ofauxin to the cytoplasm could facilitate non-polar auxin
transportby generating channel-like auxin transport routes (Wabnik
et al.,2011).
Interestingly, polar auxin transport has been recently
detectedin the charophyte Chara corallina (Boot et al., 2012) and
partialPIN-like sequence was identied in the charophyte
Spirogyrapratensis (De Smet et al., 2011). If corroborated by
future studies,this nding suggests that PIN proteins predate the
origin of landplants and could potentially play a role in polar
auxin transport incharophytes. Additionally, four and two homologs
of the auxininux carriers AUX1/LAX have been detected in the
Physcomitrella(Rensing et al., 2008) and Selaginella (Banks et al.,
2011) genomes,respectively. As for ABCB and ABCG transporters, they
predate theorigin of land plants and have been identied in
chlorophytes (DeSmet et al., 2011).
Origin of auxin signaling
One surprising feature from the genome sequences of P. patensand
S. moellendorfi is evidence for the presence of auxin
signalingmachinery identical to that in owering plants (Banks et
al., 2011;Rensing et al., 2008). In the present study, a
comprehensive searchof the marchantiophyte EST database also
reveals the presence ofgenes encoding Aux/IAA proteins, ARF
proteins, TIR1/AFB proteins,and components of the SCFTIR1 complex
(Table S1). Thus, acomplete TIR/AFB-ARF-Aux/IAA signaling cascade
was probablyalready present in the last common ancestor of land
plants. Moreimportantly, molecular function of these components
seems to bepartially conserved in land plants. The use of auxin
antagonists inangiosperms and P. patens suggests that auxin
response mediatedby TIR1, Aux/IAA and ARF proteins is an ancient
mechanism(Hayashi et al., 2008). A recent study has shown that the
mossAux/IAA proteins interact with Arabidopsis TIR1 moss
homologs
called PpAFB and that a reduction in PpAFB levels and/or
mutations
-
in Aux/IAA genes lead to an auxin-resistant phenotype (Priggeet
al., 2010). Additionally, the expression of some ARF genes
isregulated by small RNA-guided cleavage both in owering plantsand
in P. patens (Axtell et al., 2007).
Finally, genomic analyses revealed the presence of genesencoding
ABP1 and IBR5 proteins in bryophytes (Rensing et al.,2008) and
lycophytes (Banks et al., 2011), suggesting that thethree known
auxin signaling pathways were present in the lastcommon ancestor of
extant land plants.
Auxin biology in algae
What evidence does exists for an auxin signaling network
inalgae? Auxin was demonstrated to induce cell division and
interactwith cytoskeleton in the charophyte lineage (Jin et al.,
2008). Auxinalso promotes cell division and prevents the formation
of lateralbranches in rhodophytes (Yokoya and Handro, 1996). In
brown algae,which are members of an eukaryotic lineage distinct
from Viridi-plantae, IAA is required to ensure both proper
branching pattern byrelaying cellcell positional information (Le
Bail et al., 2010) andproper establishment of polarity of the
developing embryo, assuggested by the use of exogenous application
of auxin or auxintransport inhibitors (Basu et al., 2002; Sun et
al., 2004). Genomicanalyses reveal the absence of the
TIR1-Aux/IAA-ARF mediated auxinsignaling pathway in green algae
(Lau et al., 2009; Rensing et al.,2008; Riano-Pachon et al., 2008).
On the contrary, putative ABP1 andIBR5 orthologs have been identied
in green algae (Lau et al., 2009;Monroe-Augustus et al., 2003) and
could account for any auxin-
TPL/TPR, PIN, and NPH3-like gene families are thus far the
onlyexamples of auxin-related genes that appeared before the
splitbetween charophytes and streptophytes (charophytes and
embryo-phytes) (Floyd et al., 2006).
Auxin was recruited independently during evolution
Examples from macro-evo-devo
In marked contrast to bryophytes that form a shoot in thehaploid
generation, vascular plants develop shoots in the
diploidgeneration. Moreover, polar auxin transport is involved in
theshoot development in owering plants, whereas it is not the
casein moss shoots in the gametophyte (Fujita et al., 2008).
However,auxin is present in P. patens shoots and was detected in
the basalpart of the gametophore stem (Bierfreund et al., 2003;
Fujita et al.,2008). These studies suggest that different
developmentalmechanisms have been recruited to produce shoots in
bryophytesand vascular plants, even if auxin could play a role in
both cases.
Another example is provided by the rooting system in
plants.Tracheophytes (vascular plants) develop roots specialized
inabsorption of water and nutrients and anchoring of the plant
tothe ground. By contrast, bryophytes have rhizoids and not
trueroots since rhizoids are not produced by root meristems. In
bothcases, auxin is involved both in the development and growth
ofroots (Sabatini et al., 1999) and rhizoids (Sakakibara et al.,
2003).Similarly to bryophytes, it has been reported that algae can
have
oid
ctiva
by
ysc
C. Finet, Y. Jaillais / Developmental Biology 369 (2012)
193126mediated signaling. The ability to infer the ancestral
developmentaltool kit of extant chlorobionts and of extant land
plants has beenmade possible by the complete genome sequencing of
several greenalgae and early-diverged lineages of land plants,
respectively(Bowman et al., 2007; Floyd and Bowman, 2007).
Unfortunately,these data do not allow us to reveal the auxin
machinery incharophytes, especially in the case of a gene absent in
green algaeand present in land plants. Class III
homeodomain-leucine zipper,
Fig. 4. Comparative development of Arabidopsis root hair cell
and Physcomitrella rhizin the root by inducing GLABRA2 (GL2) gene
expression, CAPRICE (CPC) acts as an a
SCRAMBLED (SCM) receptor is thought to respond to a cortical
layer positional cue
lipid messenger PtdIns(4,5)P2 synthesized by the PIPK5K3 enzyme.
Similarly, Phdifferentiation, whilst PIPK1 and PIPK2 are essential
for rhizoid elongation.. Contrary to the WEREWOLF (WER)
transcription factor that species non-hair fate
tor of hair fate by inducing the expression of ROOT HAIR
DEFECTIVE 6 (RHD6). The
repressing WER expression in the future hair cell. Hair cell
elongation involves the
omitrella RHD SIX-LIKE1 (RSL1) and RSL2 transcription factors
promote rhizoidrhizoids whose development and growth is also
affected by auxin(Basu et al., 2002; Klambt et al., 1992). Given
that roots andrhizoids are not homologous structures, it seems
likely that auxinhave been independently recruited.
Rather, rhizoids are thought to be homologous to root hair
cells.Their development share common features (Fig. 4) such as the
keyrole of ROOT HAIRLESS (RSL) transcription factors in specifying
thefuture hair cells (vs. non-hair cells) (Jang et al., 2011;
Menand et al.,
-
patterning of the embryo is impaired when exogenous IAA or
relevant for ARF activators, this hypothesis seems unlikely for
ARF
C. Finet, Y. Jaillais / Developmental Biology 369 (2012) 1931
27transport inhibitors are applied (Basu et al., 2002; Sun et
al.,2004). Such results raise an important question about
plantevolution in a broader sense: is it possible that embryos of
bothembryophytes and brown algae represent elaborations of
somezygotic developmental mechanism present in the last
commonancestor of these groups? If so, the involvement of IAA in
zygotepatterning would be a plesiomorphic feature that might
havebeen present in the common ancestor. Alternatively, the
auxinpathway may have been independently recruited for
embryopatterning both in brown algae and in embryophytes. The
pre-sence of IAA in brown algae, coupled with the lack of
conservationof IAA transport and signaling pathways in Ectocarpus
siliculosus(Le Bail et al., 2010), could support the independent
recruitmentof IAA in both brown algae and the green lineage.
Auxin as a main player in micro-evo-devo
In addition to its putative role in land plant radiation,
auxinwas shown to underpin morphological diversication
withinowering plants. The best-known example is the
differentialdistribution of auxin as a source of diversity of leaf
morphologyin closely related species. The current model for the
developmentof A. thaliana leaf margin protrusions involves the
accumulation ofauxin by the efux carrier PIN1 and the activity of
the growth-repressor CUC2 (Bilsborough et al., 2011). In
Brassicales, thespecies A. thaliana has simple leaves with margin
protrusions atthe base whereas Cardamine hirsuta produces dissected
leavesdivided into several leaets. Similarly to leaf margin
protrusionsin A. thaliana, the formation of leaets in C. hirsuta
requires auxinmaxima and the PIN1 protein (Barkoulas et al., 2008).
However,the output of PIN1 action differs in that auxin induces
growth of alimited number of cells at the Arabidopsis leaf margin,
as opposedto induction of growth of the entire population of cells
that willgive rise to leaets in C. hirsuta. The ability of PIN1 to
promoteleaet formation involves regulation by KNOX proteins that
areexpressed in C. hirsuta leaves, but not in those of A. thaliana
(Hayet al., 2006). Taken together, these ndings suggest that
differ-ential auxin distribution is necessary to explain
species-specicleaf shape in closely related species.
More recently, PIN1-mediated auxin activity maxima were2007) and
the one of phosphatidylinositol-4-phosphate 5-kinase(PIPK) enzymes
in promoting elongation (Kusano et al., 2008;Saavedra et al., 2011;
Stenzel et al., 2008). Similarly, auxin playsa role in the
development of both hair cells and rhizoids but doesnot act at the
same level in the developmental network. Althoughauxin positively
regulates the expression of RSL genes early duringrhizoid
specication (Jang et al., 2011), auxin is not involved in haircell
specication in Arabidopsis (Jang et al., 2011) but modulateshair
cell planar polarity (Ikeda et al., 2009). If rhizoids and root
haircells are homologous structures, these data suggest that
eitherauxin might have played a role in the development of the
rstland plant soil anchoring system and that the regulatorynetwork
diverged later between mosses and owering plants orauxin has been
recruited independently in mosses and in angios-perms but the
linkage occurred at different level in the regulatorynetwork.
A last example of convergence could be the role of auxinduring
embryonic development. As presented above, properpatterning of the
embryo in angiosperms is largely dependentupon auxin. By denition,
embryophytes have evolved an embryo,which is a zygote producing
further mitotic tissues, whereas algaehave a zygote that enters
immediately meiosis. However, somebrown algae are known to develop
an embryo, e.g., in the Fucusand Laminaria genera. In F. distichus,
it has been reported that theshown to generate leaf dissection in
tomato (Ben-Gera et al.,repressors that have limited interaction
with Aux/IAA proteins(Vernoux et al., 2011). Similarly, loss of
functional domain I motif(LxLxL) that confers transcriptional
repressor function of Aux/IAAs occurred independently several times
during evolution ofland plants (Paponov et al., 2009). However, the
moss Aux/IAAproteins that contain the non-canonical motif LxLxPP
may stillinteract with TPL (Causier et al., 2012), challenging the
idea thatloss of domain I motif LxLxL could affect Aux/IAA
function.
Auxin is an instructive molecule that triggers a
differentialdevelopmental output given its concentration. Thus,
minorchanges in auxin localization (e.g. mutations in promoters
ofbiosynthesis genes, gain of novel tissue-specic enhancers)
couldhave been responsible for important innovation at both
micro-and macro-evolutionary scale.
From the embryogenetic point of view, roots are believed tohave
evolved from primitive shoots (Gifford and Foster, 1987). In
A.2012; Koenig et al., 2009), which unravels the molecular basis
ofthe conversion from complex to simple leaves after treatmentwith
PAT inhibitors in tomato (Avasarala et al., 1996) and pea(DeMason
and Chawla, 2004). Moreover, KNOX proteins wereshown to be required
for leaet formation in tomato (Bharathanet al., 2002). Given that
dissected leaves evolved independentlyseveral times during the
evolution of angiosperms, those ndingssuggest a broad role for
auxin efux in the elaboration of morecomplex leaf forms. KNOX/auxin
interactions are similar to thoseoperating in the SAM, suggesting
that they may also be rede-ployed later in development of dissected
leaves to generateleaets. Nevertheless, further studies will be
required to addressthe question whether changes in auxin biology
are the cause orjust a carrier of information due to changes in
other regulators innatural variation.
Towards hypothetical models for body plan diversication
Very few differences in auxin-related gene content have
beenidentied between lineages in land plants, suggesting that
thecore auxin machinery was already present in the last
commonancestor of land plants. Thus, morphological innovations
withinland plants would be rather the result of evolutionary
tinkeringwith the ancestral auxin regulatory network.
The recent identication of ER-localized PIN proteins in
Arabi-dopsis (Mravec et al., 2009) has shed new light on the role
ofendoplasmic reticulum in auxin biology (Friml and Jones,
2010).Going further with this idea, we propose that changes in
thetrafcking of auxin-related proteins through the ER could
haveplayed a role in macroevolution. For example, ABP1 moss
proteinsdiffer from their homologs in owering plants in that they
lackthe ER-retention motif KDEL and they are consequently
notlocalized in the ER (Panigrahi et al., 2009). Another
noteworthypoint is that the moss genome does not contain
amidohydrolasesof the clade ILL1/ILL2/IAR3/ILL5/ILL6, whose members
meetbioinformatics criteria for ER localization (Davies et al.,
1999).
Changes in the coding region of proteins involved in
nuclearauxin signaling could have also played a role in
complicating theauxin regulatory network. The two huge ARF and
Aux/IAA genefamilies mainly evolve by changes in coding regions,
which canlead to the origin of truncated proteins. For example,
somemembers of the ARF3/4 clade have lost their
proteinproteininteraction domains during the evolution of land
plants, suggest-ing that they are not able to interact with Aux/IAA
and areconsequently insensitive to auxin (Finet et al., 2010a).
Loss ofthese domains occurred several times during evolution and
couldrepresent a way to escape the auxin signaling pathway.
Althoughthaliana, root- and shoot-specifying genetic pathways are
tightly
-
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E.M., Estelle,M., Feng, L., Finet, C., Floyd, S.K., Frommer, W.B.,
Fujita, T., Gramzow, L.,linked since repression of root development
module in the shoot isnecessary for the proper shoot development
(Long et al., 2006).Moreover, root stem cells establishment
requires some shoot-specifying components (Grigg et al., 2009).
Thus, it would bereasonable to imagine that changes (even minor) in
auxin dis-tribution, such as expansion in the basal part of the
developingembryo, could have contributed to the emergence of
roots.
Referring to the evolutionary conclusions brought by the studyof
HOX genes, Stephen Jay Gould liked to use the term hoxology.It
would be therefore timely to use the word auxology to takeinto
account the crucial role of auxin in plant evo-devo.
Acknowledgments
We would like to thank Ullas Pedmale and Teva Vernoux forhelpful
discussions. We wish to excuse to colleagues whoserelevant work has
not been cited due to space limitations.
Appendix A. Supplementary material
Supplementary data associated with this article can be found
inthe online version at
http://dx.doi.org/10.1016/j.ydbio.2012.05.039.
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